4.7 Article

RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis

Journal

DEVELOPMENT
Volume 140, Issue 14, Pages 2953-2960

Publisher

COMPANY OF BIOLOGISTS LTD
DOI: 10.1242/dev.092981

Keywords

Arabidopsis; Seed; Imprinting; Endosperm; RdDM; DNA methylation

Funding

  1. Temasek Lifesciences Laboratory at National University of Singapore
  2. Department of Biological Sciences at National University of Singapore
  3. Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry [BRAIN 03-01]
  4. JST ERATO Higashiyama Live-Holonics Project
  5. Japan Society for the Promotion of Science [7811]
  6. Direct For Biological Sciences
  7. Division Of Integrative Organismal Systems [1025830] Funding Source: National Science Foundation

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In mammals and plants, parental genomic imprinting restricts the expression of specific loci to one parental allele. Imprinting in mammals relies on sex-dependent de novo deposition of DNA methylation during gametogenesis but a comparable mechanism was not shown in plants. Rather, paternal silencing by the maintenance DNA methyltransferase 1 (MET1) and maternal activation by the DNA demethylase DEMETER (DME) cause maternal expression. However, genome-wide studies suggested other DNA methylation-dependent imprinting mechanisms. Here, we show that de novo RNA-directed DNA methylation (RdDM) regulates imprinting at specific loci expressed in endosperm. RdDM in somatic tissues is required to silence expression of the paternal allele. By contrast, the repression of RdDM in female gametes participates with or without DME requirement in the activation of the maternal allele. The contrasted activity of DNA methylation between male and female gametes appears sufficient to prime imprinted maternal expression. After fertilization, MET1 maintains differential expression between the parental alleles. RdDM depends on small interfering RNAs (siRNAs). The involvement of RdDM in imprinting supports the idea that sources of siRNAs such as transposons and de novo DNA methylation were recruited in a convergent manner in plants and mammals in the evolutionary process leading to selection of imprinted loci.

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